Bioactive Compound Synthetic Capacity and Ecological Significance of Marine Bacterial Genus Pseudoalteromonas
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Mar. Drugs 2007, 5, 220-241 Marine Drugs ISSN 1660-3397 © 2007 by MDPI www.mdpi.org/marinedrugs Review Bioactive Compound Synthetic Capacity and Ecological Significance of Marine Bacterial Genus Pseudoalteromonas John P. Bowman * Tasmania Institute of Agricultural Research, School of Agricultural Science, University of Tasmania, Sandy Bay, Private Bag 54, Hobart, Tasmania, 7001, Australia; E-mail: [email protected] Received: 27 November 2007 / Accepted: 14 December 2007 / Published: 18 December 2007 Abstract: The genus Pseudoalteromonas is a marine group of bacteria belonging to the class Gammaproteobacteria that has come to attention in the natural product and microbial ecology science fields in the last decade. Pigmented species of the genus have been shown to produce an array of low and high molecular weight compounds with antimicrobial, anti-fouling, algicidal and various pharmaceutically-relevant activities. Compounds formed include toxic proteins, polyanionic exopolymers, substituted phenolic and pyrolle-containing alkaloids, cyclic peptides and a range of bromine- substituted compounds. Ecologically, Pseudoalteromonas appears significant and to date has been shown to influence biofilm formation in various marine econiches; involved in predator-like interactions within the microbial loop; influence settlement, germination and metamorphosis of various invertebrate and algal species; and may also be adopted by marine flora and fauna as defensive agents. Studies have been so far limited to a relatively small subset of strains compared to the known diversity of the genus suggesting that many more discoveries of novel natural products as well as ecological connections these may have in the marine ecosystem remain to be made. Keywords: Pseudoalteromonas, antibiotics, biofilms, anti-fouling, marine bacteria. 1. Introduction The genus Pseudoalteromonas was described by Gauthier et al. [35] and represents a clade of marine bacteria defined on the basis of 16S rRNA gene sequence data. Originally many of the Pseudoalteromonas species that are discussed in this review were members of the genus Alteromonas Mar. Drugs 2007, 5 221 [5, 77] but Alteromonas was taxonomically re-organized based on phylogenetic analysis. Since 1995, 22 additional Pseudoalteromonas species have been described (details available at http://www.bacterio.cict.fr/p/pseudoalteromonas.html). More recently two Pseudoalteromonas species have been moved into the genus Algicola [50, 74]. The taxonomy and general features of Pseudoalteromonas (ca. 2000/2001) are covered in the 2nd edition of Bergey’s Manual of Systematic Bacteriology [8]. Possessing Gram-negative cell walls, all members of genus Pseudoalteromonas require Na+ ions, form rod-shaped cells, are motile via sheathed polar and/or unsheathed lateral flagella and possess a strictly aerobic, chemoheterotrophic metabolism. This general set of features has coined the common term “alteromonad” that could be potentially used to now describe other marine genera within class Gammaproteobacteria. Genus Pseudoalteromonas groups within a larger clade of marine taxa, located under the umbrella of order Alteromonadales that inhabit all known non-geothermal marine biomes. One interesting feature of Pseudoalteromonas is that the genus can be divided relatively cleanly into pigmented and non-pigmented species clades (Fig. 1) and that pigmentation correlates with their proclivity for natural product formation [22]. The non-pigmented species form a relatively distinct clade typified by phylogenetic shallowness between most member species. Pigmented species show greater sequence divergence and are concentrated within the other 2 major clades making up the genus (Fig. 1). With more than 2000 Pseudoalteromonas 16S rRNA gene sequences available on nucleotide sequence databases (e.g. www.ncbi.nlm.nih.gov) the described diversity of the genus still remains largely incomplete. Studies by Holmström et al. [43] found deeply pigmented strains within a marine bacterial isolate collection were effective in the inhibition of the settlement of various fouling invertebrates and algae. Based on subsequent analyses some of these isolates lead to the general conclusion that pigmented Pseudoalteromonas species possess a broad range of bioactivity associated with the secretion of extracellular compounds, several of which include pigment compounds [44]. This realization provided greater credence to earlier studies of alteromonads that this group of marine bacteria represents a rich source of biologically active substances. Non-pigmented species of Pseudoalteromonas do not appear to share the same extensiveness of bioactive compound synthesis and this may reflect their econiche distribution, which is admittedly still poorly defined. Within the limits of existing knowledge non- pigmented clade species tend to possess unusual and diverse enzymatic activities (carrageenases, chitinases, alginases, cold-active enzymes), generally broader environmental tolerance ranges (temperature, water activity and pH) and substantially greater nutritional versatility compared to the pigmented species [8]. The pigmented species also tend to have more exacting growth requirements (some require amino acids) and have peroxidase activity rather than catalase activity. 2. Ecological Significance. Marine biofilms influence the settlement of a variety of marine invertebrates and algae and may promote cellular metamorphosis. As biofilms can be quite variable in distribution and in species and chemical composition the influence they can have is complex. The activity of marine flora and fauna have been shown to be clearly positively or negatively influenced by experimental monospecific Mar. Drugs 2007, 5 222 biofilms [17, 82, 98]. This activity is believed to be due mainly to the production of antibiotic compounds as well as stimulatory chemical cues that are so far mostly uncharacterized. Figure 1. Phylogenetic tree of genus Pseudoalteromonas based on 16S rRNA gene sequences (5’-prime region, poisitions 10 to 509 E. coli equivalent). Nucleotide distances are based on the maximum likelihood algorithm and the tree clustered using the Neighbor- joining procedure (Phylip v. 3.67; Joe Felsenstein; http://evolution.genetics.washington.edu/ phylip.html). Clades within the genus are demarcated in different color type. Species in green are non-pigmented species. Species in blue and purple, as well as P. ruthenica are predominantly brightly-pigmented species (see Table 1). Mar. Drugs 2007, 5 223 Several known Pseudoalteromonas species and likely many other described and undescribed bacterial species can influence the reproductive success of various marine fauna and flora due to the production of natural anti-fouling substances [17] (Table 1). A survey by Holmström et al. [42] found that the effectiveness of different Pseudoalteromonas species to prevent settlement of fouling invertebrate larvae and algal spores varies considerably (Figure 2). Figure 2. The inhibition of invertebrate larvae and algal spore settlement by different Pseudoalteromonas species. Data adapted from Holmström et al. [42]. 100 80 60 40 Surface settlement (%) 20 0 P. rubra P. citrea Control P. tunicata P. aurantia P. ulvae P. piscicida P. luteoviolacea Balanus amphitrite larvae Hydroides elegans larvae Polysiphonia sp. spores Ulva lactuca spores It was generally observed that algal dwelling species were particularly effective in preventing biofouling suggesting the ability is important for their survival in the marine ecosystem and likely required for effective colonization of various surfaces, especially the surfaces of macroalgal species. P. luteoviolacea [34], P. aurantia [33]; P. citrea [31, 79], P. tunicata, and P. ulvae [20-22, 45] are of particular interest as the host of compounds these species form are essentially produced to prevent biofilm residents becoming overwhelmed by other colonizing, potentially fouling species [26, 38]. Species resistant to natural antibiotics have an advantage in colonization [83] though presumably due to the array of compounds that may be formed no one species is likely to have such an edge that they always become numerically dominant in a given econiche. The result could be that antibiotic- producing strains and development of synergisms within biofilm communities may actually encourage the formation of multi-species biofilms. This protects the biofilm community from being overgrown by a single species as well as reducing invasion by other species [12]. The complex community formed has the advantage in that there is an inherent increase in the efficiency of nutrient acquisition, enhanced tolerance to toxic compounds and physicochemical stresses, and presumably excellent opportunities for genetic exchange [78]. Ironically, Pseudoalteromonas species are highly effective biofilm formers and thus may potentially cause biofouling issues [87], however it is still unknown Mar. Drugs 2007, 5 224 whether their presence controls the type and accumulation level of biofouling species beyond specific habitats such as the surface of marine algal species. Quorum-sensing mechanisms may play an important role in the influencing settlement and subsequent biofilm formation [19, 46] though it is unknown to what extent quorum sensing molecules influence antibiotic production. Table 1. Bioactive compound production and associated activities by described Pseudoalteromonas species. Species Pigmented Source Bioactive compoundsb Inhibitory activities [other a activities]b P. aliena + (melanin)